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Association between Dentitheca habereri (Cnidaria: Hydrozoa) and twozoanthidsC. G. Di Camillo a; M. Bo a; S. Puce a; G. Bavestrello a

a DiSMar, Università Politecnica delle Marche, Ancona, Italy

First published on: 18 January 2010

To cite this Article Di Camillo, C. G., Bo, M., Puce, S. and Bavestrello, G.(2010) 'Association between Dentitheca habereri(Cnidaria: Hydrozoa) and two zoanthids', Italian Journal of Zoology, 77: 1, 81 — 91, First published on: 18 January 2010(iFirst)To link to this Article: DOI: 10.1080/11250000902740962URL: http://dx.doi.org/10.1080/11250000902740962

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Association between Dentitheca habereri (Cnidaria: Hydrozoa) and twozoanthids

C. G. DI CAMILLO*, M. BO, S. PUCE, & G. BAVESTRELLO

DiSMar, Universita Politecnica delle Marche, Ancona, Italy

(Received 19 June 2008; accepted 9 January 2009)

AbstractDentitheca habereri is a leptomedusan hydroid forming large colonies on the fringing reefs of the Bunaken National Park(North Sulawesi, Indonesia). The hydroid is generally associated with two zoanthid species, Parazoanthus gracilis andParazoanthus sp. Colonies lacking zoanthid epibionts are rare and generally smaller (8–10 cm). When associated withParazoanthus sp., the hydroid colonies are fan-shaped and may exceed 1 m in width. In contrast, when D. habereri iscolonised by the large polyps of Parazoanthus gracilis, the host colonies are smaller and the branching is irregular.

Keywords: Dentitheca habereri, zoanthids, epibiosis, distribution

Introduction

Hydroids often live as epibionts on other organisms

or, conversely, act as a substrate for both vagile and

sessile species (Bavestrello et al. 1996; Zintzen et al.

2008). These associations often lead to very close

relationships ranging from mutualism to parasitism

(Boero & Bouillon 2005; Puce et al. 2008).

Although large hydroid colonies are often a suitable

substrate for smaller hydroids, they rarely host other

cnidarians, particularly anthozoans. In the Adriatic

Sea, the octocoral Cornularia cornucopiae and occa-

sionally small anemones can surround the base of

the stalk of Eudendrium colonies, but no exclusive

relationship with the host appears to be established

(Di Camillo, unpublished).

Zoanthids are common epibionts of different

organisms (Acosta et al. 2005; Sinniger et al.

2005) including gorgonians and black corals (West

1979), but relationships with hydroids are poorly

documented (Table I). Parazoanthus gracilis lives on

the thecate hydroid Dentitheca habereri, Parazoanthus

tunicans is associated with Plumularia sp.,

Parazoanthus dichroicus grows on Plumularia ramsay,

Parazoanthus douglasi on an unidentified hydroid,

and a Parazoanthus or Epizoanthus species is

associated with the aglaopheniid Macrorhynchia

philippina (Haddon & Shackleton 1891; Duerden

1900; Stechow 1909, 1913; Tischbierek 1929; Van

Gemerden-Hoogeveen 1965; West 1979; Inaba

1982; Muirhead & Ryland 1984; Ryland &

Muirhead 1993; Hirohito 1995; Burnett et al. 1997;

Sinniger et al. 2005). Moreover, Calder (personal

communication) observed that Dentitheca habereri

from the Indo-Pacific Ocean and D. dendritica from

the Caribbean Sea are covered by undetermined

zoanthids (Table I). Finally, Billard (1913, Planche

II, Fig. 23) shows the hydroid Plumularia crater

partially covered by a zoanthid, but this association

was not mentioned in the text. These data show that

the only hydroids known as hosting zoanthids belong

to the closely related families Plumulariidae and

Aglaopheniidae, suggesting a certain degree of

specialisation in this relationship.

The first hydroid species recorded associated to a

zoanthid was Dentitheca habereri (Stechow 1909),

but the correct interpretation of this association had

a complex story. Plumularia (5Dentitheca) habereri

was described by Stechow (1909) based on material

collected in the Sagami Bay by Haberer in 1903.

The author misunderstood the association with

the zoanthid, describing numerous, small and

*Correspondence: C. G. Di Camillo, Dipartimento di Scienze del Mare, Universita Politecnica delle Marche, Via Brecce Bianche, I-60131 Ancona, Italy.

Tel: +39 071 2204649. Fax: +39 071 2204650. Email: c.dicamillo@univpm.it

Italian Journal of Zoology, March 2010; 77(1): 81–91

ISSN 1125-0003 print/ISSN 1748-5851 online # 2010 Unione Zoologica Italiana

DOI: 10.1080/11250000902740962

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unbranched hydroid colonies growing on a large

gorgonian. In 1892, Inaba had already described an

unidentified Plumularia from Misaki (Sagami Bay),

depicting this hydroid partially covered by an

epibiont he identified as a sponge. In 1913,

Stechow considered Inaba’s hydroid as belonging

to D. habereri and reinterpreted the type material

of this species as being a large, branched and

Table I. Survey of associations reported in literature (numbers indicate records shown in Figure 4).

Hydroid Zoanthid Localities Author and year No.

Plumularia habereri Parazoanthus gracilis Ebisina, Misaki (Sagami Bay) Carlgren 1934 1

Plumularia habereri Parazoanthus gracilis North Sulawesi (Indonesia) Sinniger et al. 2005 2

Plumularia habereri Parazoanthus gracilis

(Epizoanthus cnidosus)

Ito, Sagami bay (Japan) Tieshbierek 1929 3

?Plumularia habereri Not specified Curacao, Carribean Van Gemerden-Hoogevan 1965 4

Plumularia habereri var.

mediolineata

Not specified Indonesia Billard 1913 – Planche III,

Fig. 31

5

Plumularia habereri Not specified (identified

as a gorgonian)

Between Ito and Hatsushima,

Sagami bay (Japan)

Stechow 1909 and 1913 6

Plumularia habereri Not specified (identified

as a sponge)

Wagamura, Shishigahana,

Misaki (Japan)

Inaba 1892 7

Dentitheca habereri Parazoanthus gracilis Between Ito and Hatsushima,

Sagami bay (Japan)

Stechow 1923b 8

Dentitheca habereri Parazoanthus gracilis Sagami bay (Japan) Hirhoito 1995 9

Dentitheca habereri With undetermined

zoanthids

Off Normanby Island,

Papua New Guinea

Calder, personal communication 10

Dentitheca habereri With undetermined

zoanthids

Kapalai Island, Malaysia Calder, personal communication 11

Dentitheca habereri With undetermined

zoanthids

Tulear, Madagascar Gravier-Bonnet, personal

communication

12

Dentitheca habereri With undetermined

zoanthids

Tulear, Madagascar Pichon 1978 (Thesis) 13

Dentitheca dendritica With undetermined

zoanthids

Long Cay, Lighthouse Reef,

Belize

Calder, personal communication 14

Dentitheca dendritica With undetermined

zoanthids

West Palm Beach, Florida,

USA

Calder, personal communication 15

Plumulariid Parazoanthus gracilis

(Sidisia gracilis)

Misaki, Sagami bay (Japan) Lwowsky 1913 16

Plumularia sp. Parazoanthus tunicans Pedro Bank, Jamaica Duerden 1900 17

Plumularia sp. Parazoanthus tunicans Off La Parguera, Puerto Rico West 1979 18

Not specified Parazoanthus tunicans Utila (Honduras) Sinniger et al. 2005 19

Plumularia ramsay Parazoanthus dichroicus Channel between Mer

and Dauar (Torres Strait)

Haddon & Shackleton 1891 20

Not specified Parazoanthus dichroicus Bowden (Torres Strait) Burnett et al. 1997 21

Not specified Parazoanthus douglasi Albany Pass, Cape York

(Torres Strait)

Haddon & Shackleton 1891 22

Macrorhynchia philippina Parazoanthus or

Epizoanthus sp.

Cleveland Bay

(off Townsville, Australia)

Muirhead & Ryland 1984;

Ryland & Muirhead 1993

23

Plumularia crater ? Indonesia Billard 1913 – Planche II, Fig. 23 24

Plumularia habereri var.

attenuata

? Damar, Indonesia Billard 1913: 42, figs 34–38. 25

Plumularia habereri var.

elongata

? Borneo Billard 1913: 44, fig 35–37. 26

Plumularia habereri var.

subarmata

? North Ubian, Indonesia Billard 1913: 45, fig 38. 27

Plumularia habereri var.

mucronata

? Borneo Billard 1913: 46, fig 60,

pl 2 fig 24.

28

Plumularia ?habereri ? Baia di Cartagena, Colombia Florez Gonzalez 1983 29

Dentitheca habereri ? Guam, Micronesia Kirkendale & Calder 2003 30

Plumularia habereri ? Herald Pass, Great

Astrolabe reef, Fiji

Ryland & Gibbons 1991 31

Plumularia habereri ? Kei Islands - Samalon Island

near Ujungpandang, Sulawesi,

Schuchert 2003 32

Dentitheca habereri ? Europa Island Gravier-Bonnet, personal

communication

33

82 C. G. Di Camillo et al.

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polysiphonic hydroid colony that did not grow on

the sponge, but was instead covered by it. In 1923,

Stechow transferred his species to the genus

Dentitheca, finally recognising that the hydroid was

covered by the zoanthid Parazoanthus gracilis which

had been identified by Ferdinand Pax (Stechow

1923a).

The latter species was described by Lwowsky

(1913) as Sidisia gracilis on material collected by

Doflein in 1904 at Misaki (Sagami Bay) living on an

unidentified plumulariid hydroid. The image (Taf.

19) shows a colony very likely belonging to D.

habereri. Carlgren (1913) re-examined the descrip-

tion and drawings of Sidisia gracilis made by

Lwowsky (1913) and suggested that the zoanthid

was in all probability a Parazoanthus species.

Another specimen originating from the Haberer’s

collection and growing on a colony of D. habereri was

described by Tischbierek (1929) as Epizoanthus

cnidosus. Carlgren (1934) synonymised Epizoanthus

cnidosus with Parazoanthus gracilis and described a

Parazoanthus gracilis specimen from Ebisina (Misaki,

Sagami Bay) that was associated with D. habereri.

Billard (1913) published an illustration (Planche

III, Fig. 31) of a portion of D. habereri from

Indonesia (Pulu-Missa, Makassar, South Sulawesi)

showing small, rounded warts covering the basal

part of a branch. These structures could be

zoanthids growing on the hydroid skeleton,

although they were not mentioned in the text. Van

Gemerden-Hoogeveen (1965) studied three colo-

nies identified as D. habereri from Curacao

(Caribbean) partly covered with zoanthids, remark-

ing that the distal parts of stems, branches and

hydrocladia were free of epibionts.

Dentitheca habereri is a common hydroid on the

coral reefs of the Bunaken Marine Park (North

Sulawesi, Indonesia) where it forms large, branched

colonies generally associated two species of

Parazoanthus. The aim of this work is to describe

the relationship between this hydroid and its

epibionts.

Materials and methods

Samples of Dentitheca habereri were collected from

different sites in the Bunaken National Marine Park

(Figure 1) by SCUBA diving from November 2004

to March 2007. The reefs of the Bunaken archipe-

lago are typical fringing reefs composed of a shallow,

mainly sandy reef flat colonised by few species, the

edge of the reef, characterised by foliaceous and

branched stony corals generally subjected to strong

currents, and vertical walls with canyons and caves

showing the greatest hydroid abundance (Di

Camillo et al. 2008).

Before sampling, the colonies were photographed

and measured. Small specimens were collected

entirely, while portions were cut from large, fan-

shaped colonies. After sampling, living specimens

Figure 1. Map of sampling sites.

Association between Dentitheca habereri and two zoanthids 83

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were examined with a microscope for the identifica-

tion; drawings were made, and pictures and mea-

surements of the hydroid and their epibionts were

taken. Afterwards, the samples were fixed using 4%

neutralised formaldehyde.

For scanning electron microscopy analysis, small

portions of the hydroid were rinsed with distilled

water, then dehydrated in a graded ethanol series

and dried by means of a critical point dryer. Samples

were coated with gold-palladium in a Balzer Union

sputter-coater and examined with a Philips XL20

SEM.

Several pieces of the hydroid hosting zoanthids

were taken off and prepared to obtain resin sections.

First, samples were dehydrated in a graded ethanol

series, than embedded in Technovit 8100 resin.

Sections (10 mm) were mounted on slides and then

stained with toluidine blue; finally slides were

enclosed using Eukitt.

During February 2007, six colonies of D. habereri

associated with two species of zoanthids were tagged

and measured to obtain data on the growth rate of

the associations. Unfortunately, in January 2008

only one colony was still alive. For this specimen,

area, maximum width and maximum height were

determined from underwater photographs using the

ImageJ software and the growth rate was thereby

calculated.

Results

Description of Dentitheca habereri

Family Plumulariidae McCrady, 1859

Genus Dentitheca Stechow, 1919

Dentitheca habereri (Stechow, 1909)

Figures 2, 3. Table II.

Plumularia habereri Stechow 1909: 77, pl 6 fig 4;

Stechow 1913: 10 and 91, figs 59,60; Ryland &

Gibbons 1991: 532: fig. 5; Schuchert 2003: 211,

fig. 60;

?Plumularia habereri van Gemerden-Hoogeeveen

1965: 60, figs 34–36.

?Plumularia habereri Florez Gonzalez 1983: 121,

figs 38,39.

Dentitheca habereri Stechow 1920: 41; Stechow

1923a: 227; Stechow 1923b: 18; Hirohito 1995:

259, fig 87a–c; Kirkendale & Calder 2003: 167 and

179; Pichon 1978: 432.

Plumularia habereri var. attenuata Billard 1913: 42,

figs 34–38.

Plumularia habereri var. elongata Billard 1913: 44,

figs 35–37.

Plumularia habereri var. subarmata Billard 1913: 45,

fig 38.

Plumularia habereri var. mediolineata Billard 1913:

45, fig 39, pl 3 fig 31.

Plumularia habereri var. mucronata Billard 1913: 46,

fig 60, pl 2 fig 24.

Material examined

Bunaken National Marine Park, North Sulawesi,

(Indonesia): Bualo, 20–25 m; Sachiko, 40 m; Siladen,

20–50 m; Mandolin, 25 m; Depan Kampung, 5–

30 m; Likuan, 5–30 m; Mike’s Point, 5–30 m.

Other examined material

Coel. No. 4059, Zoologisch Museum Amsterdam,

Plumularia habereri var. mediolineata, type v/d var.,

Billard – Siboga Expedition, Stat. 80. – Nr. 4781

Sammlung Haberer – Zoologische Staatssammlung

Muenchen (portion of the type material of P.

habereri described by Stechow 1909).

Figure 2. Dentitheca habereri. A, young colony not yet colonised

by epibionts; B, hydrotheca in lateral view; C, hydrotheca in

frontal view; D, particular of the hydrocladial apophysis; E,

gonothecae. Scale bars: A, 1 cm. B–D, 100 mm. E, 200 mm.

84 C. G. Di Camillo et al.

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Description

Large colonies, fan-shaped, reaching 70 cm in height

and 107 cm in width; branched up to the fourth

order; lateral branches arising from apophyses on the

auxiliary tubes. The smallest colonies (5–6 cm in

height) branched up to second order. Hydrocaulus

and main branches rigid, strongly polysiphonic;

perisarc of the tubes very thick; distal portions of

the branches monosiphonic; each tube bearing

nematothecae arranged in rows. Apophyses of

variable length, a mamelon and two nematothecae

visible on the basal part of each apophysis; a

transverse node separates the apophysis from the

branch. The first internode bearing a variable

number of nematothecae depending on its length,

the nematothecae sometimes arranged in couples.

The remaining internodes generally not segmented;

nodes, when present, transverse. Internodes bearing

alternate hydrocladial apophyses associated with two

nematothecae and a mamelon.

Hydrocladia with up to 16 uniseriate hydrothecae;

the internodes showing several internal ribs; nodes

indistinct; each internode with one hydrotheca and

three nematothecae (one median inferior and two

lateral).

Hydrothecae cylindrical, deep, the adcauline wall

completely adnate. Thecal margin almost straight or

slightly sinuous in the adcauline side and lowering

towards the adcauline side. Abcauline wall curved; a

Figure 3. SEM pictures of Dentitheca habereri. A, hydrotheca in lateral view; B, particular of a lateral nematotheca; C, portion of a fertile

colony showing gonothecae; D, particular of a gonotheca. Scale bars: A, D, 200 mm. B, 50 mm. C, 2 mm.

Table II. Measurements of D. habereri (mm).

Portions Dentitheca habereri

Diameter of cauline internodes (small colonies) 13–360

Diameter of cauline internodes (big colonies) up to 6000

Length of hydrocladial internode 450–470

Diameter of hydrocladial internode 60–120

Hydrothecae Diameter of hydrothecal margin 100–120

Length of adnate adcauline wall 190–200

Nematocysts Microbasic mastigophores 8.75–1063.75–5

Microbasic mastigophores 562.5

Lateral Upper chamber 22.5–25

Nematothecae Lower chamber 42.5–45

Median inferior Upper chamber 22.5–25

Nematothecae Lower chamber 42.5–45

Association between Dentitheca habereri and two zoanthids 85

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fold is often present just above the half height. The

internal fold is sometimes absent (see remarks). The

median inferior nematotheca placed on a promi-

nence of the internode, not reaching the theca base;

lateral nematothecae not reaching the thecal margin.

All nematothecae movable and two-chambered: the

upper chamber conical, the walls straight; the inner

wall of the upper chamber emarginate.

Gonothecae arising from the hydrocladial apo-

physes, large, tapered to base, and distally truncated;

the lateral walls curved.

Measurements (mm): see Table II.

Colour: Stems and branches shining brown,

hydrocladia brownish.

Ecology

Colonies of D. habereri were observed along vertical

cliffs from 10 to 50 m depth, but they are more

abundant from 20 to 40 m depth. This species was

mainly found in sites exposed to strong currents.

Remarks

In some specimens, the hydrocladia are shorter,

bearing nine or fewer hydrothecae, and the inter-

nodes generally do not contain internal ribs. The

hydrothecae of these colonies are cylindrical or

campanulate, and the distal hydrothecae are deeper

than the proximal ones. Moreover, these thecae are

slightly smaller (length of adnate adcauline wall 130–

160 mm; diameter of hydrothecal margin 90–

100 mm) and lack an intrathecal fold.

The distributions of Dentitheca habereri and other

hydroids associated with zoanthids are shown in

Figure 4 and Table I. The descriptions of the two

specimens reported from the Caribbean Sea (Van

Gemerden-Hoogeveen 1965; Florez Gonzalez 1983)

do not match with the characters of D. habereri and

their attribution must be considered doubtful.

Unfortunately the comparison of our specimens

with the original material was impossible because

the samples are lost. Therefore it seems likely that D.

Figure 4. Distribution of Dentitheca habereri and records of the associations reported in literature between hydroids and zoanthids. Number

correspondences are shown in Table I.

86 C. G. Di Camillo et al.

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habereri has an Indo-Pacific distribution and the

Caribbean hydroids associated with zoanthids

belong to a different species.

Associated zoanthids (Table III)

The systematics of the zoanthids associated with

hydroids appears very complex. Studies based on

molecular analyses (Sinniger et al. 2005) suggest that

these species probably belong to a separate clade.

Based on morphological criteria, in the Bunaken

Marine Park Dentitheca habereri was found associated

with two different zoanthids: Parazoanthus gracilis and

Parazoanthus sp.

Parazoanthus sp. is characterised by polyps with a

viscid surface; they are small and delicate (Table III),

with a dark red scapus and yellow tentacles

(Figure 5A–C). Foreign bodies are scarce, limited

to the capitular ridges and visible only when the

polyps are closed. This species is clearly different

from P. gracilis in colour and size of the polyps and in

the scarcity of incorporated particles.

Parazoanthus gracilis (Lwowsky, 1913) is charac-

terised by large polyps (Table III) with a long scapus

(Figure 5D–F). The coenenchyme and the polyps

are completely incrusted by calcareous sand grains

and sponge spicules that render the consistency of

the coenenchyme brittle. The tentacles are generally

dark brown, sometimes yellow. The debris coat

makes the polyps grey-coloured, but the inner

coenenchyme is dark brown. The colonies are not

viscid. The comparison with the zoanthid covering

the type material of D. habereri (Stechow, 1909)

identified as P. gracilis (Lwowsky, 1913) by

Ferdinand Pax (Stechow 1923a) revealed that the

polyps of our specimen are larger.

Figure 5. A–C, Underwater pictures of Dentitheca habereri hosting Parazoanthus sp. A, a large, fan-shaped colony; B, detail of A; C,

Parazoanthus sp. covering the hydroid up to the apex and leaving free the hydrocladia; D–F, underwater pictures of Dentitheca habereri

hosting Parazoanthus gracilis. D, colony of a hydroid with epibiontic zoanthids; E, detail of D; F, detail showing Parazoanthus gracilis

covering hydrocladia. G–I, Resin sections of D. habereri associated with zoanthids. G, longitudinal section of specimen covered with

Parazoanthus sp. Note the living coenosarc inside the hydroid skeleton (arrows); H, detail; I, transverse section of D. habereri covered with

Parazoanthus gracilis. White arrow, hydroid coenosarc; z, zoanthid tissue; s, hydroid skeleton.

Association between Dentitheca habereri and two zoanthids 87

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In the Bunaken area, colonies of D. habereri not

associated with zoanthids were small and rare, but

small colonies with few branches were found covered

with zoanthids. In the associations with both

zoanthid species, the hydroid portions covered by

the epibiont are alive as was demonstrated by the

sections showing living coenosarc within the hydroid

skeleton (Figure 5G–I).

The colonies of D. habereri associated with

Parazoanthus sp. were more numerous than those

associated with P. gracilis, representing about 70% of

all colonies. Generally, only one of the two epibionts

was present on the same hydroid colony. However,

we found a large colony of D. habereri that was

widely covered by Parazoanthus sp. but also had a

small portion covered by P. gracilis.

Parazoanthus sp. forms a continuous layer around

the hydrocaulus and the polysiphonic branches of

the hydroid colonies. In thinner portions, the

epibiont covers the main axis and grows up to

the distal apex of the branches, always leaving the

hydrocladia free (Figure 6A–C). The polyps of

the zoanthid are arranged alternately above and

below the axis. The hydroid branches protrude from

the covered areas and show living polyps. Such

covered hydroid colonies are fan-shaped, with

branches arranged almost in one plane, and reach

69 cm in height and 107 cm in width.

Dentitheca habereri forms smaller colonies when

hosting P. gracilis than when covered by

Parazoanthus sp., reaching only 31 cm in height

and 36 cm in width. Such colonies are not

fan-shaped because the branching is irregularly

three-dimensional. During their growth, the colonies

of P. gracilis cover both branches and hydrocladia,

but leave the terminal, ramified hydroid portions

free (Figure 6D,E).

The only one of the D. habereri colonies tagged in

March 2007 and still alive in January 2008 was

associated with Parazoanthus sp. Comparison of the

photographs from the two times indicates a growth

of 2.44 cm in height and 0.74 in width, with an

increase of the total surface of 63.53 cm2.

Discussion

Dentitheca habereri from Bunaken Marine Park is

almost always associated with a zoanthid: only a few

small hydroid colonies, 8–10 cm high, were recorded

free from epibiont. However, colonies less than 8 cm

high can also be covered by zoanthids: therefore,

larvae of the epibiont zoanthids settle on young

colonies of D. habereri. The zoanthids were never

observed on other substrata, suggesting that, at least

for the latter partner, the association is compulsory.

Owing to the exploitation of the hydroid skeleton

for mechanical support, the zoanthids effectively

transform themselves into erect branching organ-

isms, whilst avoiding the energetic cost of producing

their own skeleton. The advantage of this strategy for

a passive filter feeder is that, by rising well above the

substratum into faster flowing water, a larger volume

will be filtered. It remains unclear if the hydroid

benefits from this association, but it is possible that

the very large cnidae of the zoanthid provide extra

protection against predators.

Table III. Comparison of the zoanthids considered in the paper.

Parazoanthus gracilis

(present work)

Parazoanthus sp.

(present work)

E. cnidosus

Tishbierek 1929

(original description)

S. gracilis Lwowsky

1913 (original

description)

P. gracilis as

described by

Carlgren (1934)

Colour of scapus Grey Dark red – – yellowish

Colour of tentacles Generally dark brown Yellow – – –

Height of polyps (mm) 2–5 0.5–1 1.25 4.05 4.05

Diameter of polyps (mm) 1.6–3 1.6–3 1–2.8 1.8–3 3.05

Number of capitular ridges 16 12 – 18–21 16–19

Number of tentacles 32 22–24 – – 34–38

Number of mesenteries 32 ? 32 36–42 34–38

Larger nematocysts (mm) 40–47.5617.5–22.5 35–42.5615–17.5 42–52614–16 35–38615–16 44–48619–22

Colony consistence Brittle Viscid ? ? ?

Incorporated particles Coenenchyme and

capitular ridges

Scarce, limited to

the capitular ridges

Coenenchyme and

capitular ridges

Coenenchyme and

capitular ridges

Coenenchyme and

capitular ridges

Exceptions One specimen with

yellow tentacles

One specimen with

more inclusion

scattered on the

column

– – –

Locality North Sulawesi North Sulawesi Ito (Sagami Bay),

collector: Haberer

Misaki (Sagami Bay),

collector: Doflein

Ebisina, Misaki

(Sagami Bay),

collector: Gislen

88 C. G. Di Camillo et al.

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Although several hydroid species are exploited as

substratum by numerous organisms, this is uncom-

mon in species of Plumulariidae and Aglaopheniidae

that are always completely devoid of sessile epibionts

probably for the cleaning function of the widespread

nematophores (Allman 1864; Gravier-Bonnet

2004). In the case of D. habereri, it remains unknown

how the zoanthids are able to overcome the larval-

repelling role of the nematophores.

Several zoanthids are known as epibionts of

different species of branched cnidarians such as

gorgonians and antipatharians. Generally, in these

associations the colonisation leads to the death of the

host. The extreme example of this strategy occurs in

the genus Savalia living on gorgonians. When the

host is completely killed by its epibiont, the zoanthid

becomes able to produce its own skeleton deposited

on that of the sea fan, the combined skeleton

becoming extremely thick (Zibrowius 1985).

The relationship with Dentitheca is peculiar

because it seems that a sort of equilibrium is reached

between the two partners: in contrast to the

parasitism observed in the case of anthozoan

colonisation, we never found a colony of Dentitheca

completely covering and or having been killed by the

zoanthid. This is probably due to a structural

difference of gorgonians and hydroids as the

coenosarc is protected inside the perisarc tubes and

thus not in direct contact with the epibiont tissues.

In contrast, in the branched anthozoans, epibiontic

zoanthids directly contact the cellular coenenchyme

that covers the internal organic skeleton.

The relative growth of the epibiont and the host is

different in the two species of zoanthids. In

Parazoanthus gracilis, the fast growth of the hydroid

allows the distal regions with living polyps to

continuously escape from the overgrowth by the

zoanthid. The zoanthid never reaches the extremities

of the branches. In the case of Parazoanthus sp., the

relationship is more complex. This zoanthid grows

only on large branches and never covers the

hydrothecal openings. Also the influence of the two

zoanthids on the final size and shape of the hydroid

colonies differs. While the colonies infested by

Parazoanthus sp. are unusually large and charac-

terised by a fan shape and numerous ramifications,

those with P. gracilis are smaller (about one-third in

the maximal size), irregular, and with a simpler

Figure 6. A–E, Modality growth. A, colony of the hydroid covered with Parazoanthus sp.; B, enlargement of a portion; C, particular of the

distal extremities of branches showing that the zoanthid colonises the main axes leaving free the thin hydrocladia bearing polyps; D, colony

of the hydroid covered with Parazoanthus gracilis; E, particular of D.

Association between Dentitheca habereri and two zoanthids 89

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ramification pattern. This is probably due to the

different size of the polyps of the zoanthids: the

small-sized polyps of Parazoanthus sp. are able to

colonise only the branches avoiding the hydrocladia,

while the large-sized polyps of P. gracilis completely

envelop both branches and hydrocladia. Moreover,

the thin layer of Parazoanthus sp. is easily perforated

by the growing new branches, while the thick coat of

P. gracilis, embedded with abundant sediment,

probably hampers the growth of new branches.

In both cases, the result of the epibiosis is a

cooperative relationship allowing the production of a

composite organism that, especially in the case of

Parazoanthus sp., reaches unusual sizes. The two

covering strategies of the zoanthids described here

could be considered different steps in a process of

transformation of a parasitic epibiosis in a mutualis-

tic relationship.

Acknowledgements

We would like to thank Dr Bernhard Ruthensteiner

(Zoologische Staatssammlung Muenchen) for his

helpfulness and for supplying type material of

Dentitheca habereri plus related literature. We are

grateful to Dr Dale Calder and Dr Nicole Gravier-

Bonnet who provided with records of plumulariids

associated with zoanthids, and to Professor John

Ryland for bibliographic data and his constructive

criticism. Thanks to Dr Frederic Sinniger for his

comments on the manuscript and his suggestions.

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